Two-way communication between SecY and SecA suggests a brownian ratchet mechanism for protein translocation

eLife

Volumn 5, Issue MAY2016, 2016, Pages

  Allen, William John ^a   Corey, Robin Adam ^a   Oatley, Peter ^b   Sessions, Richard Barry ^a   Baldwin, Steve A ^b   Radford, Sheena E ^b   Tuma, Roman ^b   Collinson, Ian ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTEIN SECA; PROTEIN TRANSLOCASE; SECY PROTEIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN; SECA PROTEIN, BACTERIA; TRANSLOCON;

ARTICLE; BINDING AFFINITY; ENZYME KINETICS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUOROMETRY; MOLECULAR DYNAMICS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE ANALYSIS; STATIC ELECTRICITY; THERMOTOGA MARITIMA; WESTERN BLOTTING; ALPHA HELIX; BINDING SITE; CHEMISTRY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; METHANOCALDOCOCCUS; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN MOTIF; THERMODYNAMICS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID MOTIFS; BACTERIAL PROTEINS; BINDING SITES; ESCHERICHIA COLI; GENE EXPRESSION; KINETICS; METHANOCALDOCOCCUS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SEC TRANSLOCATION CHANNELS; SUBSTRATE SPECIFICITY; THERMODYNAMICS; THERMOTOGA MARITIMA;

EID: 84975225082     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15598     Document Type: Article

References (72)

1. Akimaru J, Matsuyama S, Tokuda H, Mizushima S. 1991. Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 88: 6545-6549. doi: 10.1073/pnas.88.15.6545
2. Arkowitz RA, Joly JC, Wickner W. 1993. Translocation can drive the unfolding of a preprotein domain. The EMBO Journal 12: 243-253.
3. Banroques J, Doère M, Dreyfus M, Linder P, Tanner NK. 2010. Motif III in superfamily 2 "helicases" helps convert the binding energy of ATP into a high-affinity RNA binding site in the yeast dead-box protein ded1. Journal of Molecular Biology 396: 949-966. doi: 10.1016/j.jmb.2009.12.025
4. Bauer BW, Rapoport TA. 2009. Mapping polypeptide interactions of the SecA ATPase during translocation. Proceedings of the National Academy of Sciences of the United States of America 106: 20800-20805. doi: 10.1073/pnas.0910550106
5. Bauer BW, Shemesh T, Chen Y, Rapoport TA. 2014. A "push and slide" mechanism allows sequence-insensitive translocation of secretory proteins by the SecA ATPase. Cell 157: 1416-1429. doi: 10.1016/j.cell.2014.03.063
6. Berendsen HJC, van der Spoel D, van Drunen R. 1995. GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications 91: 43-56. doi: 10.1016/0010-4655(95)00042-E
7. Bessonneau P, Besson V, Collinson I, Duong F. 2002. The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure. The EMBO Journal 21: 995-1003. doi: 10.1093/emboj/21.5.995
8. Breyton C, Haase W, Rapoport TA, Kühlbrandt W, Collinson I. 2002. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418: 662-665. doi: 10.1038/nature00827
9. Brundage L, Hendrick JP, Schiebel E, Driessen AJ, Wickner W. 1990. The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62: 649-657. doi: 10.1016/0092-8674(90)90111-Q
10. Cannon KS, Or E, Clemons WM, Shibata Y, Rapoport TA. 2005. Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. The Journal of Cell Biology 169: 219-225. doi: 10.1083/jcb.200412019
11. Collinson I, Corey RA, Allen WJ. 2015. Channel crossing: how are proteins shipped across the bacterial plasma membrane? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 370. doi: 10.1098/rstb.2015.0025
12. Corey RA, Allen WJ, Komar J, Masiulis S, Menzies S, Robson A, Collinson I. 2016. Unlocking the bacterial SecY translocon. Structure 24: 518-527. doi: 10.1016/j.str.2016.02.001
13. Deville K, Gold VA, Robson A, Whitehouse S, Sessions RB, Baldwin SA, Radford SE, Collinson I. 2011. The oligomeric state and arrangement of the active bacterial translocon. The Journal of Biological Chemistry 286: 4659-4669. doi: 10.1074/jbc.M110.175638
14. Dickson CJ, Madej BD, Skjevik AA, Betz RM, Teigen K, Gould IR, Walker RC. 2014. Lipid14: The amber lipid force field. Journal of Chemical Theory and Computation 10: 865-879. doi: 10.1021/ct4010307
15. du Plessis DJ, Berrelkamp G, Nouwen N, Driessen AJ. 2009. The lateral gate of secyeg opens during protein translocation. The Journal of Biological Chemistry 284: 15805-15814. doi: 10.1074/jbc.M901855200
16. Economou A, Wickner W. 1994. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78: 835-843. doi: 10.1016/S0092-8674(94)90582-7
17. Eisenberg D, McLachlan AD. 1986. Solvation energy in protein folding and binding. Nature 319: 199-203. doi: 10.1038/319199a0
18. Erlandson KJ, Miller SB, Nam Y, Osborne AR, Zimmer J, Rapoport TA. 2008. A role for the two-helix finger of the SecA ATPase in protein translocation. Nature 455: 984-987. doi: 10.1038/nature07439
19. Fisher AJ, Smith CA, Thoden JB, Smith R, Sutoh K, Holden HM, Rayment I. 1995. X-ray structures of the myosin motor domain of dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AIF4-. Biochemistry 34: 8960-8972. doi: 10.1021/bi00028a004
20. Gillespie DT. 1977. Exact stochastic simulation of coupled chemical reactions. The Journal of Physical Chemistry 81: 2340-2361. doi: 10.1021/j100540a008
21. Gillespie DT. 1978. Monte Carlo simulation of random walks with residence time dependent transition probability rates. Journal of Computational Physics 28: 395-407. doi: 10.1016/0021-9991(78)90060-8
22. Gogala M, Becker T, Beatrix B, Armache JP, Barrio-Garcia C, Berninghausen O, Beckmann R. 2014. Structures of the Sec61 complex engaged in nascent peptide translocation or membrane insertion. Nature 506: 107-110. doi: 10.1038/nature12950
23. Gold VA, Robson A, Clarke AR, Collinson I. 2007. Allosteric regulation of SecA: Magnesium-mediated control of conformation and activity. The Journal of Biological Chemistry 282: 17424-17432. doi: 10.1074/jbc.M702066200
24. Gold VA, Whitehouse S, Robson A, Collinson I. 2013. The dynamic action of SecA during the initiation of protein translocation. The Biochemical Journal 449: 695-705. doi: 10.1042/BJ20121314
25. Gouridis G, Karamanou S, Gelis I, Kalodimos CG, Economou A. 2009. Signal peptides are allosteric activators of the protein translocase. Nature 462: 363-367. doi: 10.1038/nature08559
26. Görlich D, Hartmann E, Prehn S, Rapoport TA. 1992. A protein of the endoplasmic reticulum involved early in polypeptide translocation. Nature 357: 47-52. doi: 10.1038/357047a0
27. Hall MC, Ozsoy AZ, Matson SW. 1998. Site-directed mutations in motif VI of escherichia coli DNA helicase II result in multiple biochemical defects: Evidence for the involvement of motif VI in the coupling of atpase and DNA binding activities via conformational changes. Journal of Molecular Biology 277: 257-271. doi: 10.1006/jmbi.1997.1614
28. Hardesty B, Kramer G. 2001. Folding of a nascent peptide on the ribosome. Progress in Nucleic Acid Research and Molecular Biology 66: 41-66. doi: 10.1016/S0079-6603(00)66026-9
29. Hartl FU, Lecker S, Schiebel E, Hendrick JP, Wickner W. 1990. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli Plasma membrane. Cell 63: 269-279. doi: 10.1016/0092-8674(90)90160-G
30. Henry GD, Maruta S, Ikebe M, Sykes BD. 1993. Observation of multiple myosin subfragment 1-adp-fluoroberyllate complexes by 19F NMR spectroscopy. Biochemistry 32: 10451-10456. doi: 10.1021/bi00090a022
31. Hizlan D, Robson A, Whitehouse S, Gold VA, Vonck J, Mills D, Kühlbrandt W, Collinson I. 2012. Structure of the secy complex unlocked by a preprotein mimic. Cell Reports 1: 21-28. doi: 10.1016/j.celrep.2011.11.003
32. Hunt JF, Weinkauf S, Henry L, Fak JJ, McNicholas P, Oliver DB, Deisenhofer J. 2002. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297: 2018-2026. doi: 10.1126/science.1074424
33. Ito K, Wittekind M, Nomura M, Shiba K, Yura T, Miura A, Nashimoto H. 1983. A temperature-sensitive mutant of E. coli exhibiting slow processing of exported proteins. Cell 32: 789-797. doi: 10.1016/0092-8674(83)90065-X
34. Jorgensen WL, Maxwell DS, Tirado-Rives J. 1996. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. Journal of the American Chemical Society 118: 11225-11236. doi: 10.1021/ja9621760
35. Josefsson LG, Randall LL. 1981. Different exported proteins in E. coli show differences in the temporal mode of processing in vivo. Cell 25: 151-157. doi: 10.1016/0092-8674(81)90239-7
36. Kainov DE, Mancini EJ, Telenius J, Lísal J, Grimes JM, Bamford DH, Stuart DI, Tuma R. 2008. Structural basis of mechanochemical coupling in a hexameric molecular motor. The Journal of Biological Chemistry 283: 3607-3617. doi: 10.1074/jbc.M706366200
37. Karamanou S, Vrontou E, Sianidis G, Baud C, Roos T, Kuhn A, Politou AS, Economou A. 1999. A molecular switch in SecA protein couples ATP hydrolysis to protein translocation. Molecular Microbiology 34: 1133-1145. doi: 10.1046/j.1365-2958.1999.01686.x
38. Kon T, Imamula K, Roberts AJ, Ohkura R, Knight PJ, Gibbons IR, Burgess SA, Sutoh K. 2009. Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nature Structural & Molecular Biology 16: 325-333. doi: 10.1038/nsmb.1555
39. Lakowicz JR. 2013. Principles of Fluorescence Spectroscopy. Springer Science & Business Media.
40. Li L, Park E, Ling J, Ingram J, Ploegh H, Rapoport TA. 2016. Crystal structure of a substrate-engaged SecY protein-translocation channel. Nature 531: 395-399. doi: 10.1038/nature17163
41. Liang FC, Bageshwar UK, Musser SM. 2009. Bacterial sec protein transport is rate-limited by precursor length: A single turnover study. Molecular Biology of the Cell 20: 4256-4266. doi: 10.1091/mbc.E09-01-0075
42. Liang FC, Bageshwar UK, Musser SM. 2012. Position-dependent effects of polylysine on sec protein transport. The Journal of Biological Chemistry 287: 12703-12714. doi: 10.1074/jbc.M111.240903
43. Lill R, Cunningham K, Brundage LA, Ito K, Oliver D, Wickner W. 1989. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. The EMBO Journal 8: 961-966.
44. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE. 2010. Improved side-chain torsion potentials for the amber ff99sb protein force field. Proteins 78: 1950-1958. doi: 10.1002/prot.22711
45. Lu J, Deutsch C. 2005. Secondary structure formation of a transmembrane segment in kv channels. Biochemistry 44: 8230-8243. doi: 10.1021/bi050372q
46. Mancini EJ, Kainov DE, Grimes JM, Tuma R, Bamford DH, Stuart DI. 2004. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 118: 743-755. doi: 10.1016/j.cell.2004.09.007
47. Mao C, Cheadle CE, Hardy SJ, Lilly AA, Suo Y, Sanganna Gari RR, King GM, Randall LL. 2013. Stoichiometry of SecYEG in the active translocase of Escherichia coli varies with precursor species. Proceedings of the National Academy of Sciences of the United States of America 110: 11815-11820. doi: 10.1073/pnas.1303289110
48. Matlack KE, Misselwitz B, Plath K, Rapoport TA. 1999. Bip acts as a molecular ratchet during posttranslational transport of prepro-alpha factor across the ER membrane. Cell 97: 553-564. doi: 10.1016/S0092-8674(00)80767-9
49. McKnight CJ, Stradley SJ, Jones JD, Gierasch LM. 1991. Conformational and membrane-binding properties of a signal sequence are largely unaltered by its adjacent mature region. Proceedings of the National Academy of Sciences of the United States of America 88: 5799-5803. doi: 10.1073/pnas.88.13.5799
50. Nouwen N, Berrelkamp G, Driessen AJ. 2009. Charged amino acids in a preprotein inhibit SecA-dependent protein translocation. Journal of Molecular Biology 386: 1000-1010. doi: 10.1016/j.jmb.2009.01.031
51. Osborne AR, Rapoport TA. 2007. Protein translocation is mediated by oligomers of the secy complex with one SecY copy forming the channel. Cell 129: 97-110. doi: 10.1016/j.cell.2007.02.036
52. Park E, Ménétret JF, Gumbart JC, Ludtke SJ, Li W, Whynot A, Rapoport TA, Akey CW. 2014. Structure of the SecY channel during initiation of protein translocation. Nature 506: 102-106. doi: 10.1038/nature12720
53. Pause A, Méthot N, Sonenberg N. 1993. The HRIGRXXR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Molecular and Cellular Biology 13: 6789-6798. doi: 10.1128/MCB.13.11.6789
54. Peyser YM, Ajtai K, Burghardt TP, Muhlrad A. 2001. Effect of ionic strength on the conformation of myosin subfragment 1-nucleotide complexes. Biophysical Journal 81: 1101-1114. doi: 10.1016/S0006-3495(01)75767-0
55. Pfeffer S, Burbaum L, Unverdorben P, Pech M, Chen Y, Zimmermann R, Beckmann R, Förster F. 2015. Structure of the native sec61 protein-conducting channel. Nature Communications 6: 8403. doi: 10.1038/ncomms9403
56. Phan BC, Peyser YM, Reisler E, Muhlrad A. 1997. Effect of complexes of ADP and phosphate analogs on the conformation of the Cys707-Cys697 region of myosin subfragment 1. European Journal of Biochemistry / FEBS 243: 636-642. doi: 10.1111/j.1432-1033.1997.00636.x
57. Piggot TJ, Sessions RB, Burston SG. 2012. Toward a detailed description of the pathways of allosteric communication in the groel chaperonin through atomistic simulation. Biochemistry 51: 1707-1718. doi: 10. 1021/bi201237a
58. Robson A, Gold VA, Hodson S, Clarke AR, Collinson I. 2009. Energy transduction in protein transport and the ATP hydrolytic cycle of SecA. Proceedings of the National Academy of Sciences of the United States of America 106: 5111-5116. doi: 10.1073/pnas.0809592106
59. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology 234: 779-815. doi: 10.1006/jmbi.1993.1626
60. Sato K, Mori H, Yoshida M, Tagaya M, Mizushima S. 1997. Short hydrophobic segments in the mature domain of proompa determine its stepwise movement during translocation across the cytoplasmic membrane of escherichia coli. The Journal of Biological Chemistry 272: 5880-5886. doi: 10.1074/jbc.272.9.5880
61. Schulze RJ, Komar J, Botte M, Allen WJ, Whitehouse S, Gold VA, Lycklama A Nijeholt JA, Huard K, Berger I, Schaffitzel C, Collinson I. 2014. Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG-SecDF-yajc-yidc. Proceedings of the National Academy of Sciences of the United States of America 111: 4844-4849. doi: 10.1073/pnas.1315901111
62. Sharma A, Leach RN, Gell C, Zhang N, Burrows PC, Shepherd DA, Wigneshweraraj S, Smith DA, Zhang X, Buck M, Stockley PG, Tuma R. 2014. Domain movements of the enhancer-dependent sigma factor drive DNA delivery into the RNA polymerase active site: Insights from single molecule studies. Nucleic Acids Research 42: 5177-5190. doi: 10.1093/nar/gku146
63. Simon SM, Peskin CS, Oster GF. 1992. What drives the translocation of proteins? Proceedings of the National Academy of Sciences of the United States of America 89: 3770-3774. doi: 10.1073/pnas.89.9.3770
64. Tomkiewicz D, Nouwen N, van Leeuwen R, Tans S, Driessen AJ. 2006. SecA supports a constant rate of preprotein translocation. The Journal of Biological Chemistry 281: 15709-15713. doi: 10.1074/jbc.M600205200
65. Ulmschneider JP, Ulmschneider MB. 2009. United Atom Lipid Parameters for Combination with the Optimized Potentials for Liquid Simulations All-Atom Force Field. Journal of Chemical Theory and Computation 5: 1803-1813. doi: 10.1021/ct900086b
66. Van den Berg B, Clemons WM, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA. 2004. X-ray structure of a protein-conducting channel. Nature 427: 36-44. doi: 10.1038/nature02218
67. van der Wolk JP, de Wit JG, Driessen AJ. 1997. The catalytic cycle of the escherichia coli SecA ATPase comprises two distinct preprotein translocation events. The EMBO Journal 16: 7297-7304. doi: 10.1093/emboj/ 16.24.7297
68. van Stelten J, Silva F, Belin D, Silhavy TJ. 2009. Effects of Antibiotics and a Proto-Oncogene Homolog on Destruction of Protein Translocator SecY. Science 325: 753-756. doi: 10.1126/science.1172221
69. Voorhees RM, Hegde RS. 2016. Structure of the Sec61 channel opened by a signal sequence. Science 351: 88-91. doi: 10.1126/science.aad4992
70. Whitehouse S, Gold VA, Robson A, Allen WJ, Sessions RB, Collinson I. 2012. Mobility of the SecA 2-helix-finger is not essential for polypeptide translocation via the SecYEG complex. The Journal of Cell Biology 199: 919-929. doi: 10.1083/jcb.201205191
71. Wolf MG, Hoefling M, Aponte-Santamaría C, Grubmüller H, Groenhof G. 2010. g_membed: Efficient insertion of a membrane protein into an equilibrated lipid bilayer with minimal perturbation. Journal of Computational Chemistry 31: 2169-2174. doi: 10.1002/jcc.21507
72. Zimmer J, Nam Y, Rapoport TA. 2008. Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455: 936-943. doi: 10.1038/nature07335